The Evolution of Sex

1. The Evolution ofSex Many groups of organisms, notably the majority of animals and plants, reproduce sexually. Why? • Bdelloid rotifer • Dandelion • Taraxacumofficinale

2. Two-fold Cost of Sex f=2 Sexual Population Asexual Population • Population with two sexes, only one of which is capable of bearing young • Population with one sex capable of bearing young t n/(2N+n) n N N kS kS kS n/(N+n) t+1 ½ 1 1 ½ This cost arises because if females contribute all resources to gametes, asexual females can produce the same number of offspring as sexual females, but avoid ‘diluting’ their genome with paternal genetic material when producing offspring. Thus, in the absence of strong selection for sex through recombination, a clonally reproducing mutant is expected to spread rapidly in a sexual population of males and females.

3. A Molecular Machinery Enabling Recombination • Sex and recombination through meiosis are confined to eukaryotes • However, a complex molecular machinery enabling homologous recombination between different DNA molecules was already present in prokaryotes long before the first eukaryotes evolved. The original function of this machinery lies in DNA repair • Three types of DNA damages are repaired in bacteria through mechanisms that involve homologous recombination: • Double strand breaks • Stalled replication forks • Single stranded DNA that arose from incomplete replication

4. A Molecular Machinery Enabling Recombination Recombinatorial repair of double strand breaks is the most relevant mechanism with respect to the evolution of sex in eukaryotes, where double strand breaks are induced during Meiosis I to initiate crossovers

5. A Molecular Machinery Enabling Recombination • Even though the main function of the recombination machinery in bacteria is to repair DNA damages, it should be stressed that already in bacteria this machinery is sometimes employed to effect sexual processes • Three such mechanisms of recombination have been identified: • Conjugation: the exchange of plasmids • Transduction: the transfer of DNA mediated by phages • Transformation: the uptake and integration of free DNA from the environment

6. Meiosis and the Alternation ofGenerations • Most eukaryotes are characterized by a life-cycle termed thealternation of generations, in which a diploid phase of cell divisions alternates with a haploid phase • Meiosis mediates the transition from a diploid generation to a haploid generation • Meiosis: • Reduces the genomic content of cells by one half • Produces haploid cells with unique combinations of genes. • Syngamy mediates the transition from a haploid generation back to a diploid generation

7. Meiosis and the Alternation ofGenerations From a purely population genetics perspective, all that recombination does is to reduce statistical associations –linkage disequilibrium– between alleles at different loci Thus, the problem of why recombination is so prevalent in natural populations boils down to the questions of what forces generate LD and under what conditions there is selection to destroy LD.

8. Meiosis and the Alternation ofGenerations • Many hypotheses have been proposed to account for the advantage of recombination: • The Deterministic Mutational Theory • The Hill-Robertson effect • Red Queen Theory

9. Meiosis and the Alternation of Generations • The Deterministic Mutational Theory • The majority of non-neutral mutations are deleterious • If a mutation has a deleterious effect, it will then usually be removed from the population by the process of natural selection • Sexual reproduction is believed to be more efficient than asexual reproduction in removing those mutations from the genome • There are two main hypotheses which explain how sex may act to remove deleterious genes from the genome. • Maintenance of mutation-free individuals • Removal of deleterious genes

10. Meiosis and the Alternation of Generations The Deterministic Mutational Theory 1. Maintenance of Mutation-free Individuals In a finite asexual population under the pressure of deleterious mutations, the random loss of individuals without such mutations is inevitable. In a sexual population, however, mutation-free genotypes can be restored by recombination of genotypes containing deleterious mutations.

11. Meiosis and the Alternation of Generations The Deterministic Mutational Theory 2. Removal of Deleterious Genes It assumes that the majority of deleterious mutations are only slightly deleterious, and affect the individual such that the introduction of each additional mutation has an increasingly large effect on the fitness of the organism. This relationship between number of mutations and fitness is known as synergistic epistasis An organism may be able to cope with a few defects, but the presence of many mutations could overwhelm its backup mechanisms. The slightly deleterious nature of mutations means that the population will tend to be composed of individuals with a small number of mutations. Sex will act to recombine these genotypes, creating some individuals with fewer deleterious mutations, and some with more. Because there is a major selective disadvantage to individuals with more mutations, these individuals die out

12. Meiosis and the Alternation of Generations The Deterministic Mutational Theory There has been much criticism of this theory, since it relies on two key restrictive conditions: The rate of deleterious mutation should exceed one per genome per generation in order to provide a substantial advantage for sex. While there is some empirical evidence for it, there is also strong evidence against it There should be strong interactions among loci (synergistic epistasis), a mutation-fitness relation for which there is only limited evidence

13. Meiosis and the Alternation of Generations The Hill-Robertson Effect If two advantageous alleles A and B occur at random. The two alleles are recombined rapidly in a sexual population but in an asexual population the two alleles must arise independently Sex could be a method by which novel genotypes are created. Since sex combines genes from two individuals, sexually reproducing populations cancombine advantageous genes while asexual populations can’t

14. Meiosis and the Alternation of Generations The Hill-Robertson Effect If, in a sexual population, two different advantageous alleles arise at different loci on a chromosome in different members of the population, a chromosome containing the two advantageous alleles can be produced within a few generations by recombination. However, should the same two alleles arise in different members of an asexual population, the only way that one chromosome can develop the other allele is to independently gain the same mutation, which would take much longer

15. Meiosis and the Alternation of Generations The Hill-Robertson Effect But these explanations depend upon the rate of mutation. If favorable mutations are so rare that each will become fixed in the population before the next arises, then sexual and asexual populations would evolve at the same rate Additionally, these explanations depend upon group selection, which most theorists maintain is a weak selective force relative to individual selection – sex is still disadvantageous to the individual due to the twofold cost of sex

16. Meiosis and the Alternation of Generations The Red-Queen Theory One of the most widely accepted theories to explain the persistence of sex is the Red Queen Hypothesis which argues that sex is maintained to assist sexual individuals in resisting parasites When an environment changes, previously neutral or deleterious alleles can become favorable. If the environment changed sufficiently rapidly, these changes in the environment can make sex advantageous for the individual. Such rapid changes in environment are caused by the co-evolution between hosts and parasites Imagine, for example that there is one gene in parasites with two alleles p and P conferring two types of parasitic ability, and one gene in hosts with two alleles h and H, conferring two types of parasite resistance, such that parasites with allele p can attach themselves to hosts with the allele h, and P to H. Such a situation will lead to cyclic changes in allele frequency -as p increases in frequency, h will be disfavored In reality, there will be several genes involved in the relationship between hosts and parasites. In an asexual population of hosts, offspring will only have the different parasitic resistance if a mutation arises. In a sexual population of hosts, however, offspring will have a new combination of parasitic resistance alleles

17. Meiosis and the Alternation of Generations The Red-Queen Theory In other words, like Lewis Carroll's Red Queen, sexual hosts are continually adapting in order to stay ahead of their parasites Evidence for this explanation for the evolution of sex is provided by comparison of the rate of molecular evolution of genes for kinases and immunoglobulins in the immune system with genes coding other proteins. The genes coding for immune system proteins evolve considerably faster Critics of the Red Queen hypothesis question whether the constantly-changing environment of hosts and parasites is sufficiently common to explain the evolution of sex

18. Mating Types Mating types are the different types of gametes that can fertilize other gametes in a sexually reproducing organism. Most species show two different mating types (male and female, + and -, a and ), but some species of fungi can present several thousands

19. Mating Types • Mating types might be the outcome of selection to: • Facilitate finding mates • In order for gametes to fertilize other gametes, they need to attract and/or be attracted by other gametes. Evolutionary models show that there may be selection for some cells to specialize in attracting gametes (by producing pheromones), while others specialize in becoming attracted (by expressing pheromone receptors) • Coordinate the inheritance of cytoplasmic genomes (for example mitochondrial genes) so as to limit competition between unrelated cytoplasmicgenomes • Fusion of isogamous gametes brings together cytoplasmic genes from different lineages that may compete to favor their own transmission to the next generation. Intragenomic conflict reduces the fitness of the organism and creates the context for the invasion of a nuclear gene that enforces the inheritance of cytoplasm from a single mother cell

20. Anisogamy and Mobile Gametes Anisogamyrefers to the production of gametes that differ (generally in size) as opposed to them being identical (isogamy) One way to explain the evolution of this asymmetry is assuming that there is a trade-off between productivity (more gametes are better than few gametes) and survival of zygotes (bigger zygotes have greater survival than smaller) This creates the context for the evolution of sexual antagonism with one of the sexes acting as a cheater that withholds resources to produce more gametes and the other sex contributing the resources withheld by the first gamete to preserve zygotic viability. This sexual conflict results in males producing small gametes that are viable only because of the resources contributed by females

21. Anisogamy and Mobile Gametes The previous model however does not take into consideration how gamete density affects the probability of fertilization. When all gametes do not find a partner to fuse with and when small gametes have a higher motility – thus increasing encountering rates with large gametes – there can be additional selective pressure for anisogamy. Thus anisogamy does not necessarily respond to the logic of sexual conflict but might be beneficial for both sexes

22. Secondary Loss of Sex Most multicellular organisms —especially animals—have a genetic system that involves obligate sex as well as male and female Because of the twofold cost of sex, this near ubiquity of sex is even more difficult to explain than explaining how sex and recombination evolved in the first place. Some species, however, have re-evolved the ability to reproduce asexually either partially or completely, thus offering important opportunities to investigate the evolutionary forces that maintain sex within populations and to test hypotheses for the advantage of recombination

23. Secondary Loss of Sex Partial loss of sexual reproduction is relatively common in multicellular organisms and characteristic of several large taxa. Some groups of animals – for example aphids, waterfleas and monogonont rotifers – reproduce mainly asexually, but under certain conditions males and females are produced and mate (facultative sex or cyclic parthenogenesis). In other groups, sexual and obligatorily asexual individuals coexist, although often with different geographical distributions ('geographical parthenogenesis').

24. Secondary Loss of Sex By contrast, complete abandonment of sexual reproduction is rare among multicellular organisms. For example, there are fewer than 100 parthenogenetic vertebrate species. The genetic basis for parthenogenetic reproduction varies among groups and includes single mutations, hybridization (possibly the only cause of parthenogenesis in vertebrates), and maternally inherited bacteria. Moreover, there is a great diversity in cytogenetic mechanisms by which offspring are produced asexually